Retinal arterial blood flow and retinal changes in patients with sepsis: preliminary study using fluorescein angiography

Kristo Erikson, Janne Henrik Liisanantti, Nina Hautala, Juha Koskenkari, Remi Kamakura, Karl Heinz Herzig, Hannu Syrjälä, Tero Ilmari Ala-Kokko, Kristo Erikson, Janne Henrik Liisanantti, Nina Hautala, Juha Koskenkari, Remi Kamakura, Karl Heinz Herzig, Hannu Syrjälä, Tero Ilmari Ala-Kokko

Abstract

Background: Although tissue perfusion is often decreased in patients with sepsis, the relationship between macrohemodynamics and microcirculatory blood flow is poorly understood. We hypothesized that alterations in retinal blood flow visualized by angiography may be related to macrohemodynamics, inflammatory mediators, and retinal microcirculatory changes.

Methods: Retinal fluorescein angiography was performed twice during the first 5 days in the intensive care unit to observe retinal abnormalities in patients with sepsis. Retinal changes were documented by hyperfluorescence angiography; retinal blood flow was measured as retinal arterial filling time (RAFT); and intraocular pressure was determined. In the analyses, we used the RAFT measured from the eye with worse microvascular retinal changes. Blood samples for inflammation and cerebral biomarkers were collected, and macrohemodynamics were monitored. RAFT was categorized as prolonged if it was more than 8.3 seconds.

Results: Of 31 patients, 29 (93%) were in septic shock, 30 (97%) required mechanical ventilation, 22 (71%) developed delirium, and 16 (51.6%) had retinal angiopathies, 75% of which were bilateral. Patients with prolonged RAFT had a lower cardiac index before (2.1 L/kg/m2 vs. 3.1 L/kg/m2, P = 0.042) and during angiography (2.1 L/kg/m2 vs. 2.6 L/kg/m2, P = 0.039). They more frequently had retinal changes (81% vs. 20%, P = 0.001) and higher intraocular pressure (18 mmHg vs. 14 mmHg, P = 0.031). Patients with prolonged RAFT had lower C-reactive protein (139 mg/L vs. 254 mg/L, P = 0.011) and interleukin-6 (39 pg/ml vs. 101 pg/ml, P < 0.001) than those with shorter RAFT.

Conclusions: Retinal angiopathic changes were more frequent and cardiac index was lower in patients with prolonged RAFT, whereas patients with shorter filling times had higher levels of inflammatory markers.

Keywords: Retinal arterial blood flow; Retinal changes; Sepsis.

Figures

Fig. 1
Fig. 1
Cardiac index according to retinal arterial filling time measured by fluorescein angiography
Fig. 2
Fig. 2
Retinal changes in patients with sepsis. (retinal hemorrhages (a), micoaneurysms (b) and vitreous hemorrhages (c))

References

    1. Kur J, Newman EA, Chan-Ling T. Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease. Prog Retin Eye Res. 2012;31(5):377–406. doi: 10.1016/j.preteyeres.2012.04.004.
    1. Liew G, Wang JJ, Mitchell P, Wong TY. Retinal vascular imaging: a new tool in microvascular disease research. Circ Cardiovasc Imaging. 2008;1(2):156–61. doi: 10.1161/CIRCIMAGING.108.784876.
    1. Rimpilainen R, Hautala N, Koskenkari J, Rimpilainen J, Ohtonen P, Mustonen P, et al. Comparison of the use of minimized cardiopulmonary bypass with conventional techniques on the incidence of retinal microemboli during aortic valve replacement surgery. Perfusion. 2011;26(6):479–86. doi: 10.1177/0267659111415564.
    1. Arnold JV, Blauth CI, Smith PL, Jagoe JR, Wootton R, Taylor KM. Demonstration of cerebral microemboli occurring during coronary artery bypass graft surgery using fluorescein angiography. J Audiov Media Med. 1990;13(3):87–90. doi: 10.3109/17453059009055108.
    1. Blauth CI, Arnold JV, Schulenberg WE, McCartney AC, Taylor KM. Cerebral microembolism during cardiopulmonary bypass: retinal microvascular studies in vivo with fluorescein angiography. J Thorac Cardiovasc Surg. 1988;95(4):668–76.
    1. Zsikai B, Bizánc L, Sztányi P, Vida G, Nagy E, Jiga L, et al. Clinically relevant sepsis model in minipigs [in Hungarian] Magy Seb. 2012;65(4):198–204. doi: 10.1556/MaSeb.65.2012.4.5.
    1. De Backer D, Donadello K, Sakr Y, Ospina-Tascon G, Salgado D, Scolletta S, et al. Microcirculatory alterations in patients with severe sepsis: impact of time of assessment and relationship with outcome. Crit Care Med. 2013;41(3):791–9. doi: 10.1097/CCM.0b013e3182742e8b.
    1. Edul VSK, Enrico C, Laviolle B, Vazquez AR, Ince C, Dubin A. Quantitative assessment of the microcirculation in healthy volunteers and in patients with septic shock. Crit Care Med. 2012;40(5):1443–8. doi: 10.1097/CCM.0b013e31823dae59.
    1. Taccone FS, Su F, Pierrakos C, He X, James S, Dewitte O, et al. Cerebral microcirculation is impaired during sepsis: an experimental study. Crit Care. 2010;14(4):R140. doi: 10.1186/cc9205.
    1. Angus DC, van der Poll T. Severe sepsis and septic shock. N Engl J Med. 2013;369(21):2063.
    1. Sato R, Nasu M. A review of sepsis-induced cardiomyopathy. J Intensive Care. 2015;3:48. doi: 10.1186/s40560-015-0112-5.
    1. Guenther U, Popp J, Koecher L, Muders T, Wrigge H, Ely EW, et al. Validity and reliability of the CAM-ICU Flowsheet to diagnose delirium in surgical ICU patients. J Crit Care. 2010;25(1):144–51. doi: 10.1016/j.jcrc.2009.08.005.
    1. Sessler CN, Gosnell MS, Grap MJ, Brophy GM, O’Neal PV, Keane KA, et al. The Richmond Agitation-Sedation Scale: validity and reliability in adult intensive care unit patients. Am J Respir Crit Care Med. 2002;166(10):1338–44. doi: 10.1164/rccm.2107138.
    1. Schorr CA, Zanotti S, Dellinger RP. Severe sepsis and septic shock: management and performance improvement. Virulence. 2014;5(1):190–9. doi: 10.4161/viru.27409.
    1. Gotts JE, Matthay MA. Sepsis: pathophysiology and clinical management. BMJ. 2016;353:i1585. doi: 10.1136/bmj.i1585.
    1. De Backer D, Verdant C, Chierego M, Koch M, Gullo A, Vincent J. Effects of drotrecogin alfa activated on microcirculatory alterations in patients with severe sepsis. Crit Care Med. 2006;34(7):1918–24. doi: 10.1097/01.CCM.0000220498.48773.3C.
    1. Sakr Y, Dubois M, De Backer D, Creteur J, Vincent J. Persistent microcirculatory alterations are associated with organ failure and death in patients with septic shock. Crit Care Med. 2004;32(9):1825–31. doi: 10.1097/01.CCM.0000138558.16257.3F.
    1. Trzeciak S, Dellinger RP, Parrillo JE, Guglielmi M, Bajaj J, Abate NL, et al. Early microcirculatory perfusion derangements in patients with severe sepsis and septic shock: relationship to hemodynamics, oxygen transport, and survival. Ann Emerg Med. 2007;49(1):88. doi: 10.1016/j.annemergmed.2006.08.021.
    1. Adam G, Schwartz B. Increased fluorescein filling defects in the wall of the optic disc cup in glaucoma. Arch Ophthalmol. 1980;98(9):1590–2. doi: 10.1001/archopht.1980.01020040442009.
    1. Schwartz B, Kern J. Age, increased ocular and blood pressures, and retinal and disc fluorescein angiogram. Arch Ophthalmol. 1980;98(11):1980–6. doi: 10.1001/archopht.1980.01020040832007.
    1. Hautala N, Kauma H, Rajaniemi SM, Sironen T, Vapalahti O, Pääkkö E, et al. Signs of general inflammation and kidney function are associated with the ocular features of acute Puumala hantavirus infection. Scand J Infect Dis. 2012;44(12):956–62. doi: 10.3109/00365548.2012.700119.
    1. MacCormick IJ, Beare NA, Taylor TE, Barrera V, White VA, Hiscott P, et al. Cerebral malaria in children: using the retina to study the brain. Brain. 2014;137(Pt 8):2119–42. doi: 10.1093/brain/awu001.
    1. Cernea D, Răsceanu A, Bârjoveanu F, Berteanu C. Retinopathy in severe acute pancreatitis [in Romanian] Oftalmologia. 2009;53(3):123–9.
    1. Hayreh SS, Weingeist TA. Experimental occlusion of the central artery of the retina. I. Ophthalmoscopic and fluorescein fundus angiographic studies. Br J Ophthalmol. 1980;64(12):896–912. doi: 10.1136/bjo.64.12.896.

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅